A phylogenetic and proteomic reconstruction of eukaryotic chromatin evolution

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Grau-Bové, Xavier | Navarrete, Cristina | Chiva, Cristina | Pribasnig, Thomas | Antó, Meritxell | Torruella, Guifré | Galindo, Luis, Javier | Franz Lang, B. | Moreira, David | López-Garcia, Purificación | Ruiz-Trillo, Iñaki | Schleper, Christa | Sabidó, Eduard | Sebé-Pedrós, Arnau

Edité par CCSD ; Nature -

International audience. Histones and associated chromatin proteins have essential functions in eukaryotic genomeorganization and regulation. Despite this fundamental role in eukaryotic cell biology, we lack aphylogenetically comprehensive understanding of chromatin evolution. Here, we combinecomparative proteomics and genomics analysis of chromatin in eukaryotes and archaea.Proteomics uncovers the existence of histone post-translational modifications in archaea.However, archaeal histone modifications are scarce, in contrast with the highly conserved andabundant marks we identify across eukaryotes. Phylogenetic analysis reveals that chromatin-associated catalytic functions (for example, methyltransferases) have pre-eukaryotic origins,whereas histone mark readers and chaperones are eukaryotic innovations. We show that furtherchromatin evolution is characterized by expansion of readers, including capture by transposableelements and viruses. Overall, our study infers detailed evolutionary history of eukaryoticchromatin: from its archaeal roots, through the emergence of nucleosome-based regulation in theeukaryotic ancestor, to the diversification of chromatin regulators and their hijacking by genomicparasites.

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